Independent effects of sham laparotomy and anesthesia on hepatic microRNA expression in rats

BMC Research Notes

Nathanael Raschzok³  Igor M Sauer³  Stefan G Tullius¹  John Iacomini⁴  Peter Neuhaus³  Christof Dame⁵  Sven Jonas²  Mehmet Haluk Morgül²  Anja Reutzel-Selke³  Steffen Lippert³  Annekatrin Leder³  Hannes Sallmon⁵  Wiebke Werner³ 

[1]Division of Transplant Surgery and Transplant Surgery Research Laboratory, Brigham and Women’s Hospital and Harvard Medical School, Boston, USA

[2]Department of Visceral, Transplantation, Thoracic, and Vascular Surgery, Universitätsklinikum Leipzig, Leipzig, Germany

[3]General, Visceral, and Transplantation Surgery, Experimental Surgery and Regenerative Medicine, Campus Virchow Klinikum, Charité - Universitätsmedizin Berlin, Berlin, Germany

[4]Molecular Cardiology Research Institute, Tufts University School of Medicine and Tufts Medical Center, Sackler School of Biomedical Sciences, Boston, USA

[5]Department of Neonatology, Campus Virchow Klinikum, Charité - Universitätsmedizin Berlin, Berlin, Germany

关键词: Surgical stress;    Sham laparotomy;    microRNA;    Liver regeneration;    Hepatectomy;   

Others  :  1127333
DOI  :  10.1186/1756-0500-7-702

 received in 2013-12-19, accepted in 2014-10-02,  发布年份 2014

【 摘 要 】

Background

Studies on liver regeneration following partial hepatectomy (PH) have identified several microRNAs (miRNAs) that show a regulated expression pattern. These studies involve major surgery to access the liver, which is known to have intrinsic effects on hepatic gene expression and may also affect miRNA screening results. We performed two-third PH or sham laparotomy (SL) in Wistar rats to investigate the effect of both procedures on miRNA expression in liver tissue and corresponding plasma samples by microarray and qRT-PCR analyses. As control groups, non-treated rats and rats undergoing anesthesia only were used.

Results

We found that 49 out of 323 miRNAs (15%) were significantly deregulated after PH in liver tissue 12 to 48 hours postoperatively (>20% change), while 45 miRNAs (14%) were deregulated following SL. Out of these miRNAs, 10 miRNAs were similarly deregulated after PH and SL, while one miRNA showed opposite regulation. In plasma, miRNA upregulation was observed for miR-133a and miR-133b following PH and SL, whereas miR-100 and miR-466c were similarly downregulated following anesthesia and surgery.

Conclusions

We show that miRNAs are indeed regulated by sham laparotomy and anesthesia in rats. These findings illustrate the critical need for finding appropriate control groups in experimental surgery.

【 授权许可】

   
2014 Werner et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Michalopoulos GK: Liver regeneration. J Cell Physiol 2007, 213:286-300.
• [2]Taub R: Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 2004, 5:836-847.
• [3]Lau WY, Lai EC, Lau SH: The current role of neoadjuvant/adjuvant/chemoprevention therapy in partial hepatectomy for hepatocellular carcinoma: a systematic review. Hepatobiliary Pancreat Dis Int 2009, 8:124-133.
• [4]Primrose JN: Surgery for colorectal liver metastases. Br J Cancer 2010, 102:1313-1318.
• [5]Fausto N, Campbell JS, Riehle KJ: Liver regeneration. Hepatology 2006, 43(2 Suppl 1):45-53.
• [6]Raschzok N, Werner W, Sallmon H, Billecke N, Dame C, Neuhaus P, Sauer IM: Temporal expression profiles indicate a primary function for microRNA during the peak of DNA replication after rat partial hepatectomy. Am J Physiol Regul Integr Comp Physiol 2011, 300:R1363-R1372.
• [7]Chen H, Sun Y, Dong R, Yang S, Pan C, Xiang D, Miao M, Jiao B: Mir-34a is upregulated during liver regeneration in rats and is associated with the suppression of hepatocyte proliferation. PLoS One 2011, 6:e20238.
• [8]Yuan B, Dong R, Shi D, Zhou Y, Zhao Y, Miao M, Jiao B: Down-regulation of miR-23b may contribute to activation of the TGF-β1/Smad3 signalling pathway during the termination stage of liver regeneration. FEBS Lett 2011, 585:927-934.
• [9]Castro RE, Ferreira DM, Zhang X, Borralho PM, Sarver AL, Zeng Y, Steer CJ, Kren BT, Rodriques CM: Identification of microRNAs during rat liver regeneration after partial hepatectomy and modulation by ursodeoxycholic acid. Am J Physiol Gastrointest Liver Physiol 2010, 299:G887-G897.
• [10]Shu J, Kren BT, Xia Z, Wong PY, Li L, Hanse EA, Min MX, Li B, Albrecht JH, Zeng Y, Subramanian S, Steer CJ: Genomewide microRNA down-regulation as a negative feedback mechanism in the early phases of liver regeneration. Hepatology 2011, 54:609-619.
• [11]Song G, Sharma AD, Roll GR, Ng R, Lee AY, Blelloch RH, Frandsen NM, Willenbring H: MicroRNAs control hepatocyte proliferation during liver regeneration. Hepatology 2010, 51:1735-1743.
• [12]Marquez RT, Wendlandt E, Galle CS, Keck K, McCaffrey AP: MicroRNA-21 is upregulated during the proliferative phase of liver regeneration, targets Pellino-1, and inhibits NF-kappaB signaling. Am J Physiol Gastrointest Liver Physiol 2010, 298:G535-G541.
• [13]Zhou J, Ju W, Wang D, Wu L, Zhu X, Guo Z, He X: Down-regulation of microRNA-26a promotes mouse hepatocyte proliferation during liver regeneration. PLoS One 2012, 7:e33577.
• [14]Chaveles I, Zaravinos A, Habeos IG, Karavias DD, Maroulis I, Spandidos DA, Karavias D: MicroRNA profiling in murine liver after partial hepatectomy. Int J Mol Med 2012, 29:747-755.
• [15]Juskeviciute E, Vadigepalli R, Hoek JB: Temporal and functional profile of the transcriptional regulatory network in the early regenerative response to partial hepatectomy in the rat. BMC Genomics 2008, 9:527. BioMed Central Full Text
• [16]Dransfeld O, Gehrmann T, Köhrer K, Kircheis G, Holneicher C, Häussinger D, Wettstein M: Oligonucleotide microarray analysis of differential transporter regulation in the regenerating rat liver. Liver Int 2005, 25:1243-1258.
• [17]Mauleon I, Lombard MN, Muñoz-Alonso MJ, Cañelles M, Leon J: Kinetics of myc-max-mad gene expression during hepatocyte proliferation in vivo: Differential regulation of mad family and stress-mediated induction of c-myc. Mol Carcinog 2004, 39:85-90.
• [18]Higgins GM, Anderson RM: Experimental pathology of the liver: restoration of the liver of the white rat following partial surgical removal. Arch Pathol 1931, 12:186-202.
• [19]Kirschner MB, Kao SC, Edelman JJ, Armstrong NJ, Vallely MP, van Zandwijk N, Reid G: Haemolysis during sample preparation alters microRNA content in plasma. PLoS One 2011, 6:e24145.
• [20]Lakner AM, Bonkovsky HL, Schrum LW: microRNAs: fad or future of liver disease. World J Gastroenterol 2011, 17:2536-2542.
• [21]Qin Y, Yu Y, Dong H, Bian X, Guo X, Dong S: MicroRNA 21 inhibits left ventricular remodeling in the early phase of rat model with ischemia-reperfusion injury by suppressing cell apoptosis. Int J Med Sci 2012, 9:413-423.
• [22]Truettner JS, Alonso OF, Bramlett HM, Dietrich WD: Therapeutic hypothermia alters microRNA responses to traumatic brain injury in rats. J Cereb Blood Flow Metab 2011, 31:1897-1907.
• [23]Aldrich BT, Frakes EP, Kasuya J, Hammond DL, Kitamoto T: Changes in expression of sensory organ-specific microRNAs in rat dorsal root ganglia in association with mechanical hypersensitivity induced by spinal nerve ligation. Neuroscience 2009, 164:711-723.
• [24]Kren BT, Wong PY, Shiota A, Zhang X, Zeng Y, Steer CJ: Polysome trafficking of transcripts and microRNAs in regenerating liver after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol 2009, 297:G1181-G1192.
• [25]Chen X, Murad M, Cui YY, Yao LJ, Venugopal SK, Dawson K, Wu J: miRNA regulation of liver growth after 50% partial hepatectomy and small size grafts in rats. Transplantation 2011, 91:293-299.
• [26]Zhang Y, Liao Y, Wang D, He Y, Cao D, Zhang F, Dou K: Altered expression levels of miRNAs in serum as sensitive biomarkers for early diagnosis of traumatic injury. J Cell Biochem 2011, 112:2435-2442.
• [27]Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006, 38:228-233.
• [28]Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF: Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci U S A 2006, 103:8721-8726.
• [29]Turchinovich A, Weiz L, Langheinz A, Burwinkel B: Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011, 39:7223-7233.
• [30]Wang K, Zhang S, Weber J, Baxter D, Galas DJ: Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 2010, 38:7248-7259.
• [31]Edmands SD, Hall AC, Ladow E: MicroArray analyses of genes regulated by Isoflurane anesthesia in vivo: a novel approach to identifying potential preconditioning mechanisms. Anesth Analg 2013, 116:589-595.
• [32]Ibrahim RB, Wilson JG, Thorsby ME, Edwards DJ: Effect of buprenorphine on CYP3A4 activity in rat and human liver microsomes. Life Sci 2000, 66:1293-1298.
• [33]Saussele T, Burk O, Blievernicht JK, Klein K, Nussler N, Nussler A, Hengstler JG, Eichelbaum M, Schwab M, Zanger UM: Selective induction of human hepatic cytochromes P450 2B6 and 3A4 my metamizole. Clin Pharmacol Ther 2007, 82:265-274.
• [34]Cheung L, Gustavsson C, Norstedt G, Tollet-Egnell P: Sex-different and growth hormone-regulated expression of microRNA in rat liver. BMC Mol Biol 2009, 10:13. BioMed Central Full Text
• [35]Shapiro MD, Bagley J, Latz J, Godwin JG, Ge X, Tullius SG, Iacomini J: MicroRNA expression data reveals a signature of kidney damage following ischemia reperfusion injury. PLoS One 2011, 6:e23011.
• [36]Farid WR, Pan Q, van der Meer AJ, de Ruiter PE, Ramakrishnaiah V, de Jonge J, Kwekkeboom J, Janssen HL, Metselaar HJ, Tilanus HW, Kazemier G, van der Laan LJ: Hepatocyte-derived microRNAs as serum biomarkers of hepatic injury and rejection after liver transplantation. Liver Transpl 2012, 18:290-297.
• [37]Starkey Lewis PJ, Dear J, Platt V, Simpson KJ, Craig DG, Antoine DJ, French NS, Dhaun N, Webb DJ, Costello EM, Neoptolemos JP, Moggs J, Goldring CE, Park BK: Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology 2011, 54:1767-1776.